Who governs science?

Traditionally, science holds itself to account, primarily through internal systems of peer review. But the recent retraction of two papers on stem-cell research by the journal Nature highlights weaknesses in this self-regulatory framework that scientists need to address

To err is human, so why should science be any different? The frailties of science can be easy to overlook because it remains one of humankind’s greatest cultural and intellectual achievements; working hand in hand with technology, it has transformed our understanding of the world and our capacity to shape it. But as any scientist will tell you, the daily grind of research is often laborious and repetitive and regularly punctuated by failure — either through error or miscalculation, or when our cherished theories cannot withstand the pitiless exactitude of experiment. What keeps us going are the moments of revelation or insight that every now and then swell the heart and the head with a warm pulse of satisfaction. Those small victories are all the more important because science is an intensely competitive career; the endless struggles for funding or the space to publish in the most acclaimed journals, which have failure rates as high as 80 or 90%, means that there are demons of disappointment crouching in every laboratory.

The human side of science was thrown into harsh relief by news on the 5th of August of the suicide of Japanese stem cell researcher Yoshiki Sasai. Sasai was a senior coauthor on two papers published in January this year by the high-profile journal Nature that reported a remarkable breakthrough: the generation of stem-cells by subjecting mouse cells to mild stresses such as pressure or acidic conditions, a procedure dubbed stimulus-triggered acquisition of pluripotency (STAP). But soon after publication the claims made in the papers came under intense scrutiny; there were concerns about reproducibility, a key test of any scientific report, and accusations of image manipulation and plagiarism. By the beginning of April an investigation by the RIKEN Center for Developmental Biology (CDB) where most of the work had been carried out found the lead author Haruko Obokata guilty of misconduct for having manipulated data with the intent to deceive. Sasai was cleared of misconduct but criticised in the investigation report for not properly checking the experimental data. On 2nd July both papers were formally retracted by Nature for reasons of plagiarism. A month later a serious and unfortunate incident became a desperate human tragedy when Sasai took his own life.

The retraction of scientific papers due to misconduct or the discovery of inadvertent error is nothing new. It is part and parcel of the human messiness of science. Occasions such as this, where the initial publication was announced with much fanfare and the unravelling has been attended by a shocking loss of life, run the risk of provoking an exaggerated response but is it important to bear in mind that only a tiny percentage of published papers — somewhere around 0.1% (though exact numbers are difficult to determine) — are withdrawn. That said, retractions and the reasons behind them should be monitored closely by the scientific community and efforts to do so are already being made, for example through the work of the Retraction Watch website set up by Ivan Oransky and Adam Marcus, or the insightful analyses of Ferric Fang and Arturo Casadevall. The relatively rapid reversal of publication of the STAP papers might be seen as evidence of a system of self-regulation that is working well but there are still questions that need to be asked.

In the aftermath of Nature’s retraction there were calls for the journal to publish the comments of the referees who assessed the manuscripts from Obokata and coworkers prior to publication. But the editor-in-chief Philip Campbell resisted; according to David Cyranoski’s report in Nature’s News & Comment section (which is editorially independent of the journal), Campbell has said that “publication of referees’ comments has been considered, but that the disadvantages — which include potential misinterpretations and the desire of many referees to keep their comments confidential — have prevented the journal from embracing this.” I have no doubt that Campbell is considering the ramifications of this case very seriously. The decision not to reveal the referees’ comments likely reflects the confidentiality that they were promised by the standing policy of the journal but, given the widespread attention that the now infamous case has attracted — a known risk in the high-stakes game that prestige journals play — I think this refusal is a mis-step. The journal’s fear of ‘misinterpretation’ might be rooted in the legitimate concerns of the publisher but is likely to rub off on the rest of the scientific community. The danger is that it looks as if we are closing our doors to the world outside, hoping they will be satisfied with scientists’ reassurance that “we know best”.

Arguably in this case transparency should trump the journal’s prerogative but there exists no authoritative scientific body or procedure that could oblige Nature — the publication of a private company — to release the referees’ reports. This strikes me as a potentially serious weakness in the conduct of scientific research, much of which depends on public funding, and which in turn depends on public trust.

There is no easy solution to this problem. The scientific community is a loose association of individuals and organisations — universities and research institutions, funding bodies, journals, publishers, learned societies and government departments. No-one is in charge and the blurred boundaries between these various sectors make the scientific community a fuzzily defined entity (which is why the actions of one sector can so easily be attributed to others). That structure, or rather, lack of structure has not been arrived at by design but reflects the organic emergence of the scientific enterprise over the past several hundred years from the work of skilled amateurs and groups of scholars with university and courtly affiliations. It poses challenges for good governance but is at the same time a source of great strength. Increased public investment in the 20th century may have stimulated the expansion and professionalisation of science but its roots retain their vigour; though the pressures of competition can lead to selfish behaviour, the amateur ethos that pervades research facilitates the ready exchange of ideas and reagents, and sustains a generous culture in which many take on significant workloads for no remuneration beyond their basic salary, such as writing, reviewing and editing of scientific papers, and assessing applications for funding. For many scientists, myself included, this ethos one of the most prized features of the research enterprise because it engenders real community spirit.

From the outside that community can at times appear hermetically sealed. In part that is simply a reflection of the focus and specialisation needed to probe nature’s deepest secrets but scientists should be mindful of losing sight of the wider world in which they operate. The transformation of research from an activity conducted by a few fortunate or well-connected individuals to one that is largely supported by public or charitable sources brings a responsibilities that scientists ignore at their peril. As a community we need to be open — open for dialogue and open for inspection, even if that sometimes entails the discomfort of exposing our human frailties.

But if no-one it in charge, how are standards to be enforced? For now regulation is the shared responsibility of individuals and organisations through arrangements that can at best be described as ad hoc. Low retraction rates may suggest that the mechanism of self-correction are effective — no conceivable system is ever going to catch all offenders — but the fall-out from the STAP retractions is a sorrowful reminder that there are no grounds for complacency. Though an extreme case, it is nevertheless a manifestation of structural problems within the methodology of science that have been discussed elsewhere. A perceptive 2012 analysis by Fang and Casadevall identified imbalances in the career structure and incentivisation of scientists as core difficulties, but although framed as a call for reform, their study concludes by simply calling for a ‘conversation’ among scientists about what changes to implement.

That conversation is certainly important but needs to broaden out to include the public, whose trust we have to maintain. It also needs to arrive at practical measures. Let me suggest one, even if it is not very original. The rapidity with which the STAP papers unravelled despite the rigour that Nature claims for its review procedures may be an embarrassment for the journal but also shows the value of access for improving the scrutiny of science. Though a subscription journal, Nature’s long-standing reputation has earned it a huge readership, which permitted many eyes to examine the details of the research, far more than the few that had read the manuscript before publication. The high-profile of the paper, boosted by accompanying reports and press-releases, helped to gather attention that, in the end proved critical, in both senses of the word.

Not every paper of the thousands published every year can expect such attention but access is the key. Open access, a model for scholarly publishing that makes the research literature available to read for free, is already on the rise, propelled by the ability of the internet to facilitate the worldwide dissemination of information. It is a model that challenges traditional publishing businesses but one that is moving with the unstoppable tide of technological change and finding favour with governments around the world seeking to maximise the value that can be gleaned from publicly-funded research. The value of open access lies not only in the sharing of information but in opening up the research literature for inspection by anyone who takes an interest.

Arguably that openness should not be confined to the published paper. Proper scrutiny will requires that the underlying data be made available. This is a non-trivial problem given the huge variety of data formats produced by modern research, and the truly astonishing rates that it is generated by some large-scale projects, such as genome sequencing or the hunt for sub-atomic particles, but is it one that experimenters and funding bodies (including Research Councils UK here in Britain) are already beginning to address. As well as facilitating the exposure of errors, the requirement to deposit the data supporting research papers should also create an additional hurdle for fraudsters.

There is a case too for opening up the processes of peer review, already begun by some journals. Though an important component of scientific quality control, peer review is hardly free from error. By tradition the identity of reviewers is concealed from the authors of submitted papers but while this enables reviewers to critique freely — an important safeguard particularly — the cloak of anonymity can be abused by reviewers too lazy or preoccupied to do a thorough job or those seeking to settle scores or gain a competitive advantage. It has been argued that peer review reports (and any response from authors) should be published, even if reviewer identities are still concealed, since this would encourage a more professional approach to the task.

Moves to greater openness will enable the scientific community to take complete, collective responsibility for quality control and help to build trust in science outside the confines of academia. In the long run, we scientists cannot hope to continue to govern ourselves, not at public expense, unless we are fully prepared to be held to account.